Bacteria Can Aid Aphids Against Predation and Parasitism

Aphids are among the most destructive plant pests. The small, sap-sucking insects are the bane of many a farmer and gardener. Typically soft bodied and without obvious weapons, aphids seem defenseless. So how do these tiny little morsels defend themselves from predators and other enemies? They do it with a little help from some unusual allies, the most famous of which are ants. Some ant species actually “farm” aphids by protecting them from predators in exchange for the honeydew they produce — a classic textbook-example of mutualism. But some aphid species are also protected by much smaller and less obvious defenders — endosymbiotic bacteria.

Meredith Swett Walker

“Endosymbiotic” bacteria live inside their hosts (“endo” means “inside” or “within” in Greek), and they have mutually beneficial relationships with their hosts. These bacteria are usually transmitted from mother to offspring during reproduction. Scientists studying endosymbiotic bacteria in insects have discovered that they do some amazing things for the pea aphid (Acyrthosiphon pisum) by protecting their aphid hosts from predation AND from parasitism.

The pea aphid feeds on plants in the legume family, including agriculturally important crops such as alfalfa, peas, and clover. A parasitic wasp, Aphidius ervi, and the convergent lady beetle (Hippodamia convergens) are two major natural enemies of the aphid. The wasp inserts its egg into an aphid, and when the egg hatches, the wasp larva gradually consumes the aphid from the inside. The lady beetle on the other hand is simply a voracious aphid predator.

Both species are sometimes used by farmers as biological-control agents seeking to manage aphids on their crops. But the aphids have a biological control tactic of their own. Their endosymbiotic bacteria can kill both the wasp and the lady beetle, albeit by very different means.

Pea aphids (Acyrthosiphon pisum) are aided by bacteria against lady beetles and parasitoid wasps that prey on them. Photo by Joseph Berger, Bugwood.org

In the case of the wasps, parasitizing the wrong aphid can mean death for their offspring. If a wasp parasitizes an aphid that’s been infected with the endosymbiotic bacterium Hamiltonella defensa, the wasp larva dies after hatching and the aphid lives on despite having a dead larva in its body cavity.

Scientists do not yet know exactly how H. defensa kills the wasp larva, but Dr. Kerry Oliver, assistant professor at the University of Georgia, and his colleagues have discovered another interesting twist that may explain it. H. defensa is often infected itself with a bacteriophage virus. It appears that the virus — not the endosymbiotic bacteria — produces a toxin that kills the wasp larva. Wasp larvae in aphids that are infected with H. defensa that lack the virus are just as likely to survive and kill their hosts as are larvae in aphids that lack H. defensa altogether. There even appears to be more than one strain of the virus, and some strains kill wasp larvae faster than others. Dr. Oliver and colleagues are continuing to work on this complex knot of a relationship between aphid, bacteria, and virus.

H. defensa, along with another endosymbiotic bacterium, Serratia symbiotica, is also involved in aphid defense against lady beetle predation. Researchers in Dr. Nicole Gerardo’s lab at Emory University examined the survival and development of convergent lady beetle larvae that ate aphids infected with endosymbiotic bacteria versus uninfected aphids and found a significant difference. Those that fed on infected aphids were less likely to survive through to pupation, emerge as adults, and reproduce.

But how does that benefit the aphid since it has already been eaten? That’s the tricky part of the story.

Most of the time, aphids reproduce by parthenogenesis, a form of asexual reproduction in which unfertilized eggs develop into embryos. This means that aphids essentially clone themselves. And because aphids tend to cluster and don’t move very far as long as food is available, most of the aphids in a given small area are not just related to each other, they are genetically identical.

This cloning and clustering behavior allows for “kin selection” to occur. Kin selection is an evolutionary strategy in which an individual increases its fitness by aiding the survival and reproduction of its relatives, even if it comes at a cost to its own survival and reproduction. So even though an aphid infected with endosymbiotic bacteria gets eaten by the lady beetle larva, that larva is more likely to die and fail to reproduce, thus reducing the population of predators around to eat the aphid’s extremely close relatives — its clones.

An example of science coming full circle: One of the endosymbiotic bacteria, Hamiltonella defensa, was named after W.D. Hamilton, a preeminent evolutionary biologist. One of Hamilton’s most important contributions was “Hamilton’s Rule,” an algebraic equation that describes kin selection.

Multicolored Asian lady beetles (Harmonia axyridis) such as this one are often used for biological control of pea aphids. Photo by Scott Bauer, USDA Agricultural Research Service, Bugwood.org.

Dr. Jennifer Kovacs, an assistant professor at Spelman College, and an undergraduate student named Candice Gaul have found similar effects of endosymbiotic bacteria in the multicolored Asian lady beetle (Harmonia axyridis), an Asian species that was introduced in North America to control aphids.

The relationship between endosymbiotic bacteria, aphids, and their parasites and predators is obviously complex. But the most exciting thing about this work may be the effects of endosymbionts throughout a food chain, and the implications of these effects for management of aphid pests.

“The most obvious implication is that symbionts that protect against parasitoids may influence whether or not biological control programs are effective,” said Dr. Oliver.

The same is likely true of endosymbiotic bacteria that protect against lady beetle predation, as lady beetles are also used for biological control. Most of the research described here has been done in the laboratory, but Dr. Oliver and colleagues are also examining endosymbiotic bacteria in aphids in the field. Different aphid populations carry different species of endosymbiotic bacteria. This raises the possibility that farmers that want to use A. ervi wasps or H. convergens lady beetles as biological-control agents for pea aphids might be able to choose the most effective agents according to which endosymbiotic bacteria are present in their aphid populations.

The interplay between viruses, bacteria, aphids, parasites, and predators illustrates just how complex species interactions can be, and how research on insect ecology and evolution can inform pest management. The case of the pea aphid and its bacteria is not unique. Endosymbiotic microorganisms are common in insects, and most insects are subject to predation, parasitism, or both. It is likely that endosymbionts that help defend their hosts are also common, which could be a fascinating avenue for future research.

Meredith Swett Walker is a former avian endocrinologist who now studies the development and behavior of two juvenile humans in the high desert of western Colorado. When she is not handling her research subjects, she writes about science and nature. You can read her work on her blogs http://picahudsonia.com and https://citizenbiologist.com or follow her on Twitter at @mswettwalker.